Understanding and exploiting 5T4 oncofoetal glycoprotein expression

Seminars in Cancer Biology

Volumn 29, Issue C, 2014, Pages 13-20

  Stern, Peter L ^a   Brazzatti, Julie ^a   Sawan, Saladin ^a   McGinn, Owen J ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

5T4 oncofoetal antigen; 5T4 immunotherapy; CXC12 chemokine; Epithelial mesenchymal transition; Wnt signalling

Indexed keywords

5T4 FAB STAPHYLOCOCCUS ENTEROTOXIN A; 5T4 ONCOFETAL GLYCOPROTEIN; ALPHA INTERFERON; ANTIBODY CONJUGATE; ANTINEOPLASTIC AGENT; BETA CATENIN; CHEMOKINE RECEPTOR CXCR4; CYTOKINE; IMMUNOMODULATING AGENT; MODIFIED VACCINIA VIRUS ANKARA 5T4 VACCINE; MONOCLONAL ANTIBODY A1 MONOMETHYLLAURISTAN F CONJUGATE; NAPTUMOMAB ESTAFENATOX; ONCOFETAL ANTIGEN; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG; WNT PROTEIN; CANCER VACCINE; CXCL12 PROTEIN, HUMAN; CXCR4 PROTEIN, HUMAN; MEMBRANE PROTEIN; ONCOFETAL ANTIGENS; PLACENTA PROTEIN; TROPHOBLASTIC GLYCOPROTEIN 5T4, HUMAN; TUMOR ANTIGEN; TUMOR MARKER;

ACUTE LYMPHOBLASTIC LEUKEMIA; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER IMMUNIZATION; CANCER IMMUNOTHERAPY; CANCER PROGNOSIS; CHEMOTAXIS; COLORECTAL CARCINOMA; DRUG SAFETY; DRUG TARGETING; DRUG TOLERABILITY; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; IMMUNOGENICITY; KIDNEY CARCINOMA; MELANOMA; MONOTHERAPY; NONHUMAN; OVARY CANCER; PROSTATE CARCINOMA; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; STOMACH CANCER; TUMOR GROWTH; GENE EXPRESSION REGULATION; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; PHYSIOLOGY; WNT SIGNALING PATHWAY;

ANTIGENS, NEOPLASM; CANCER VACCINES; CHEMOKINE CXCL12; CHEMOTAXIS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MEMBRANE GLYCOPROTEINS; MOLECULAR TARGETED THERAPY; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PREGNANCY PROTEINS; RECEPTORS, CXCR4; TUMOR MARKERS, BIOLOGICAL; WNT SIGNALING PATHWAY;

EID: 84927577635     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2014.07.004     Document Type: Review

References (73)

1. Hole N., Stern P.L. A 72kD trophoblast glycoprotein defined by a monoclonal antibody. Br J Cancer 1988, 57(3):239-246.
2. Southall P.J., Boxer G.M., Bagshawe K.D., Hole N., Bromley M., Stern P.L. Immunohistological distribution of 5T4 antigen in normal and malignant tissues. Br J Cancer 1990, 61(1):89-95.
3. Stern P. Immunotherapies targeting 5T4 oncofoetal glycoprotein. Bench to bedside immunotherapy of cancers 2014, Vol. 2. Springer, Berlin, [chapter 23].
4. Hole N., Stern P.L. Isolation and characterization of 5T4, a tumour-associated antigen. Int J Cancer 1990, 45(1):179-184.
5. Shaw D.M., Woods A.M., Myers K.A., Westwater C., Rahi-Saund V., Davies M.J., et al. Glycosylation and epitope mapping of the 5T4 glycoprotein oncofoetal antigen. Biochem J 2002, 363(Pt 1):137-145.
6. Boyle J.M., Grzeschik K.H., Heath P.R., Morten J.E., Stern P.L. Trophoblast glycoprotein recognised by monoclonal antibody 5T4 maps to human chromosome 6q14-q15. Hum Genet 1990, 84(5):455-458.
7. Myers K.A., Rahi-Saund V., Davison M.D., Young J.A., Cheater A.J., Stern P.L. Isolation of a cDNA encoding 5T4 oncofetal trophoblast glycoprotein. An antigen associated with metastasis contains leucine-rich repeats. J Biol Chem 1994, 269(12):9319-9324.
8. Bella J., Hindle K.L., McEwan P.A., Lovell S.C. The leucine-rich repeat structure. Cell Mol Life Sci 2008, 65(15):2307-2333.
9. Zhao Y., Malinauskas T., Harlos K., Jones E.Y. Structural insights into the inhibition of Wnt signaling by cancer antigen 5T4/Wnt-activated inhibitory factor 1. Structure 2014, 22(4):612-620.
10. Carsberg C.J., Myers K.A., Evans G.S., Allen T.D., Stern P.L. Metastasis-associated 5T4 oncofoetal antigen is concentrated at microvillus projections of the plasma membrane. J Cell Sci 1995, 108(Pt 8):2905-2916.
11. Carsberg C.J., Myers K.A., Stern P.L. Metastasis-associated 5T4 antigen disrupts cell-cell contacts and induces cellular motility in epithelial cells. Int J Cancer 1996, 68(1):84-92.
12. Awan A., Lucic M.R., Shaw D.M., Sheppard F., Westwater C., Lyons S.A., et al. 5T4 interacts with TIP-2/GIPC: a PDZ protein, with implications for metastasis. Biochem Biophys Res Commun 2002, 290(3):1030-1036.
13. King K.W., Sheppard F.C., Westwater C., Stern P.L., Myers K.A. Organisation of the mouse and human 5T4 oncofoetal leucine-rich glycoprotein genes and expression in foetal and adult murine tissues. Biochim Biophys Acta 1999, 1445(3):257-270.
14. Woods A.M., Wang W.W., Shaw D.M., Ward C.M., Carroll M.W., Rees B.R., et al. Characterization of the murine 5T4 oncofoetal antigen: a target for immunotherapy in cancer. Biochem J 2002, 366(Pt 1):353-365.
15. Nieto M.A., Cano A. The epithelial-mesenchymal transition under control: global programs to regulate epithelial plasticity. Semin Cancer Biol 2012, 22(5-6):361-368.
16. Barrow K.M., Ward C.M., Rutter J., Ali S., Stern P.L. Embryonic expression of murine 5T4 oncofoetal antigen is associated with morphogenetic events at implantation and in developing epithelia. Dev Dyn 2005, 233(4):1535-1545.
17. Ward C.M., Barrow K., Woods A.M., Stern P.L. The 5T4 oncofoetal antigen is an early differentiation marker of mouse ES cells and its absence is a useful means to assess pluripotency. J Cell Sci 2003, 116(Pt 22):4533-4542.
18. Ward C.M., Eastham A.M., Stern P.L. Cell surface 5T4 antigen is transiently upregulated during early human embryonic stem cell differentiation: effect of 5T4 phenotype on neural lineage formation. Exp Cell Res 2006, 312(10):1713-1726.
19. Eastham A.M., Spencer H., Soncin F., Ritson S., Merry C.L., Stern P.L., et al. Epithelial-mesenchymal transition events during human embryonic stem cell differentiation. Cancer Res 2007, 67(23):11254-11262.
20. Spencer H.L., Eastham A.M., Merry C.L., Southgate T.D., Perez-Campo F., Soncin F., et al. E-cadherin inhibits cell surface localization of the pro-migratory 5T4 oncofetal antigen in mouse embryonic stem cells. Mol Biol Cell 2007, 18(8):2838-2851.
21. Southgate T.D., McGinn O.J., Castro F.V., Rutkowski A.J., Al-Muftah M., Marinov G., et al. CXCR4 mediated chemotaxis is regulated by 5T4 oncofetal glycoprotein in mouse embryonic cells. PLoS ONE 2010, 5(4):e9982.
22. Christopherson K.W., G.Hangoc, Mantel C.R., Broxmeyer H.E. Modulation of hematopoietic stem cell homing and engraftment by CD26. Science 2004, 305(5686):1000-1003.
23. Balkwill F. The significance of cancer cell expression of the chemokine receptor CXCR4. Semin Cancer Biol 2004, 14(3):171-179.
24. Burger J.A., Kipps T.J. CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood 2006, 107(5):1761-1767.
25. Vandercappellen J., Van Damme J., Struyf S. The role of CXC chemokines and their receptors in cancer. Cancer Lett 2008, 267(2):226-244.
26. Nagasawa T., Nakajima T., Tachibana K., Iizasa H., Bleul C.C., Yoshie O., et al. Molecular cloning and characterization of a murine pre-B-cell growth-stimulating factor/stromal cell-derived factor 1 receptor: a murine homolog of the human immunodeficiency virus 1 entry coreceptor fusin. Proc Natl Acad Sci USA 1996, 93(25):14726-14729.
27. Burns J.M., Summers B.C., Wang Y., Melikian A., Berahovich R., Miao Z., et al. A novel chemokine receptor for SDF-1 and I-TAC involved in cell survival: cell adhesion, and tumor development. J Exp Med 2006, 203(9):2201-2213.
28. Marchese A. Assessment of degradation and ubiquitination of CXCR4, a GPCR regulated by EGFR family members. Methods Mol Biol 2006, 327:139-145.
29. Ganju R.K., Brubaker S.A., Meyer J., Dutt P., Yang Y., Qin S., et al. The alpha-chemokine: stromal cell-derived factor-1alpha, binds to the transmembrane G-protein-coupled CXCR-4 receptor and activates multiple signal transduction pathways. J Biol Chem 1998, 273(36):23169-23175.
30. Zhang J., Sarkar S., Yong V.W. The chemokine stromal cell derived factor-1 (CXCL12) promotes glioma invasiveness through MT2-matrix metalloproteinase. Carcinogenesis 2005, 26(12):2069-2077.
31. Marchese A., Raiborg C., Santini F., Keen J.H., Stenmark H., Benovic J.L. The E3 ubiquitin ligase AIP4 mediates ubiquitination and sorting of the G protein-coupled receptor CXCR4. Dev Cell 2003, 5(5):709-722.
32. Marinov G. Trafficking and functional interactions of the oncofoetal trophoblast glycoprotein 5T4 2012, Institute of Cancer Sciences, University of Manchester, Manchester.
33. Hay D.L., Poyner D.R., Sexton P.M. GPCR modulation by RAMPs. Pharmacol Ther 2006, 109(1-2):173-197.
34. McGinn O.J., Marinov G., Sawan S., Stern P.L. CXCL12 receptor preference, signal transduction, biological response and the expression of 5T4 oncofoetal glycoprotein. J Cell Sci 2012, 125(Pt 22):5467-5478.
35. Crazzolara R., Kreczy A., Mann G., Heitger A., Eibl G., Fink F.M., et al. High expression of the chemokine receptor CXCR4 predicts extramedullary organ infiltration in childhood acute lymphoblastic leukaemia. Br J Haematol 2001, 115(3):545-553.
36. van Zelm M.C., van der Burg M., de Ridder D., Barendregt B.H., de Haas E.F., Reinders M.J., et al. Ig gene rearrangement steps are initiated in early human precursor B cell subsets and correlate with specific transcription factor expression. J Immunol 2005, 175(9):5912-5922.
37. Moorman A.V., Ensor H.M., Richards S.M., Chilton L., Schwab C., Kinsey S.E., et al. Prognostic effect of chromosomal abnormalities in childhood B-cell precursor acute lymphoblastic leukaemia: results from the UK Medical Research Council ALL97/99 randomised trial. Lancet Oncol 2010, 11(5):429-438.
38. Castro F.V., McGinn O.J., Krishnan S., Marinov G., Li J., Rutkowski A.J., et al. 5T4 oncofetal antigen is expressed in high risk of relapse childhood pre-B acute lymphoblastic leukemia and is associated with a more invasive and chemotactic phenotype. Leukemia 2012, 26(7):1487-1498.
39. van den Berg H., de Groot-Kruseman H.A., Damen-Korbijn C.M., de Bont E.S., Schouten-van Meeteren A.Y., Hoogerbrugge P.M. Outcome after first relapse in children with acute lymphoblastic leukemia: a report based on the Dutch Childhood Oncology Group (DCOG) relapse all 98 protocol. Pediatr Blood Cancer 2011, 57(2):210-216.
40. Nusse R. Wnt signaling in disease and in development. Cell Res 2005, 15(1):28-32.
41. Gordon M.D., Nusse R. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 2006, 281(32):22429-22433.
42. Huelsken J., Behrens J. The Wnt signalling pathway. J Cell Sci 2002, 115(Pt 21):3977-3978.
43. Pourreyron C., Reilly L., Proby C., Panteleyev A., Fleming C., McLean K., et al. Wnt5a is strongly expressed at the leading edge in non-melanoma skin cancer, forming active gradients, while canonical Wnt signalling is repressed. PLoS ONE 2012, 7(2):e31827.
44. Ho H.Y., Susman M.W., Bikoff J.B., Ryu Y.K., Jonas A.M., Hu L., et al. Wnt5a-Ror-Dishevelled signaling constitutes a core developmental pathway that controls tissue morphogenesis. Proc Natl Acad Sci USA 2012, 109(11):4044-4051.
45. McEwen D.G., Peifer M. Wnt signaling: moving in a new direction. Curr Biol 2000, 10(15):R562-R564.
46. Sheldahl L.C., Slusarski D.C., Pandur P., Miller J.R., Kuhl M., Moon R.T. Dishevelled activates Ca2+ flux: PKC, and CamKII in vertebrate embryos. J Cell Biol 2003, 161(4):769-777.
47. van Amerongen R., Nusse R. Towards an integrated view of Wnt signaling in development. Development 2009, 136(19):3205-3214.
48. Kagermeier-Schenk B., Wehner D., Ozhan-Kizil G., Yamamoto H., Li J., Kirchner K., et al. Waif1/5T4 inhibits Wnt/beta-catenin signaling and activates noncanonical Wnt pathways by modifying LRP6 subcellular localization. Dev Cell 2011, 21(6):1129-1143.
49. Pukrop T., Binder C. The complex pathways of Wnt 5a in cancer progression. J Mol Med (Berl) 2008, 86(3):259-266.
50. Weeraratna A.T., Jiang Y., Hostetter G., Rosenblatt K., Duray P., Bittner M., et al. Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 2002, 1(3):279-288.
51. Yamamoto H., Kitadai Y., Yamamoto H., Oue N., Ohdan H., Yasui W., et al. Laminin gamma2 mediates Wnt5a-induced invasion of gastric cancer cells. Gastroenterology 2009, 137(1):242-252. 252.e1-6.
52. Clark C.E., Nourse C.C., Cooper H.M. The tangled web of non-canonical Wnt signalling in neural migration. Neurosignals 2012, 20(3):202-220.
53. Wrigley E., McGown A.T., Rennison J., Swindell R., Crowther D., Starzynska T., et al. 5T4 oncofetal antigen expression in ovarian carcinoma. Int J Gynecol Cancer 1995, 5(4):269-274.
54. Peng C., Zhang X., Yu H., Wu D., Zheng J. Wnt5a as a predictor in poor clinical outcome of patients and a mediator in chemoresistance of ovarian cancer. Int J Gynecol Cancer 2011, 21(2):280-288.
55. Badiglian Filho L., Oshima C.T., De Oliveira Lima F., De Oliveira Costa H., De Sousa Damiao R., Gomes T.S., et al. Canonical and noncanonical Wnt pathway: a comparison among normal ovary, benign ovarian tumor and ovarian cancer. Oncol Rep 2009, 21(2):313-320.
56. Dimitriadis A., Vincan E., Mohammed I.M., Roczo N., Phillips W.A., Baindur-Hudson S. Expression of Wnt genes in human colon cancers. Cancer Lett 2001, 166(2):185-191.
57. Ghosh M.C., Collins G.D., Vandanmagsar B., Patel K., Brill M., Carter A., et al. Activation of Wnt5A signaling is required for CXC chemokine ligand 12-mediated T-cell migration. Blood 2009, 114(7):1366-1373.
58. Tamura M., Sato M.M., Nashimoto M. Regulation of CXCL12 expression by canonical Wnt signaling in bone marrow stromal cells. Int J Biochem Cell Biol 2011, 43(5):760-767.
59. Mulryan K., Ryan M.G., Myers K.A., Shaw D., Wang W., Kingsman S.M., et al. Attenuated recombinant vaccinia virus expressing oncofetal antigen (tumor-associated antigen) 5T4 induces active therapy of established tumors. Mol Cancer Ther 2002, 1(12):1129-1137.
60. Smyth L.J., Elkord E., Taher T.E., Jiang H.R., Burt D.J., Clayton A., et al. CD8 T-cell recognition of human 5T4 oncofetal antigen. Int J Cancer 2006, 119(7):1638-1647.
61. Elkord E., Burt D.J., Drijfhout J.W., Hawkins R.E., Stern P.L. CD4+ T-cell recognition of human 5T4 oncofoetal antigen: implications for initial depletion of CD25+ T cells. Cancer Immunol Immunother 2008, 57(6):833-847.
62. Elkord E., Dangoor A., Burt D.J., Southgate T.D., Daayana S., Harrop R., et al. Immune evasion mechanisms in colorectal cancer liver metastasis patients vaccinated with TroVax (MVA-5T4). Cancer Immunol Immunother 2009, 58(10):1657-1667.
63. Amato R.J., Hawkins R.E., Kaufman H.L., Thompson J.A., Tomczak P., Szczylik C., et al. Vaccination of metastatic renal cancer patients with MVA-5T4: a randomized, double-blind, placebo-controlled phase III study. Clin Cancer Res 2010, 16(22):5539-5547.
64. Harrop R., Shingler W., Kelleher M., de Belin J., Treasure P. Cross-trial analysis of immunologic and clinical data resulting from phase I and II trials of MVA-5T4 (TroVax) in colorectal: renal, and prostate cancer patients. J Immunother 2010, 33(9):999-1005.
65. Binder D.C., Schreiber H. Dual blockade of PD-1 and CTLA-4 combined with tumor vaccine effectively restores T-cell rejection function in tumors-letter. Cancer Res 2014, 74(2):632. discussion 635.
66. Ott P.A., Hodi F.S., Robert C. CTLA-4 and PD-1/PD-L1 blockade: new immunotherapeutic modalities with durable clinical benefit in melanoma patients. Clin Cancer Res 2014, 19(19):5300-5309.
67. Hedlund G., Forsberg G., Nederman T., Sundstedt A., Dahlberg L., Tiensuu M. Tumour targeted superantigens. Fusion protein technologies for biopharmaceuticals: applications and challenges 2013, John Wiley & Sons, Inc., Hoboken, NJ, USA. S. Schmidt (Ed.).
68. Shaw D.M., Connolly N.B., Patel P.M., Kilany S., Hedlund G., Nordle O., et al. A phase II study of a 5T4 oncofoetal antigen tumour-targeted superantigen (ABR-214936) therapy in patients with advanced renal cell carcinoma. Br J Cancer 2007, 96(4):567-574.
69. Eisen T., Hedlund G., Forsberg G., Hawkins R. Naptumomab estafenatox: targeted immunotherapy with a novel immunotoxin. Curr Oncol Rep 2014, 16(2):370.
70. Damelin M., Geles K.G., Follettie M.T., Yuan P., Baxter M., Golas J., et al. Delineation of a cellular hierarchy in lung cancer reveals an oncofetal antigen expressed on tumor-initiating cells. Cancer Res 2011, 71(12):4236-4246.
71. Sapra P., Damelin M., Dijoseph J., Marquette K., Geles K.G., Golas J., et al. Long-term tumor regression induced by an antibody-drug conjugate that targets 5T4: an oncofetal antigen expressed on tumor-initiating cells. Mol Cancer Ther 2013, 12(1):38-47.
72. Martinez Arias A., Brickman J.M. Gene expression heterogeneities in embryonic stem cell populations: origin and function. Curr Opin Cell Biol 2011, 23(6):650-656.
73. Chen S., Wang J., Gou W.F., Xiu Y.L., Zheng H.C., Zong Z.H., et al. The involvement of RhoA and Wnt-5a in the tumorigenesis and progression of ovarian epithelial carcinoma. Int J Mol Sci 2013, 14(12):24187-24199.